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      Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon

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          Stress experienced during early life may have lasting effects on the immune system, with impacts on health and disease dependent on the nature and duration of the stressor. The epigenome is especially sensitive to environmental stimuli during early life and represents a potential mechanism through which stress may cause long-lasting health effects. However, the extent to which the epigenome responds differently to chronic vs acute stressors is unclear, especially for non-mammalian species. We examined the effects of acute stress (cold-shock during embryogenesis) and chronic stress (absence of tank enrichment during larval-stage) on global gene expression (using RNA-seq) and DNA methylation (using RRBS) in the gills of Atlantic salmon ( Salmo salar) four months after hatching. Chronic stress induced pronounced transcriptional differences, while acute stress caused few lasting transcriptional effects. However, both acute and chronic stress caused lasting and contrasting changes in the methylome. Crucially, we found that acute stress enhanced transcriptional immune response to a pathogenic challenge (bacterial lipopolysaccharide, LPS), while chronic stress suppressed it. We identified stress-induced changes in promoter and gene-body methylation that were associated with altered expression for a small proportion of immune-related genes, and evidence of wider epigenetic regulation within signalling pathways involved in immune response. Our results suggest that stress can affect immuno-competence through epigenetic mechanisms, and highlight the markedly different effects of chronic larval and acute embryonic stress. This knowledge could be used to harness the stimulatory effects of acute stress on immunity, paving the way for improved stress and disease management through epigenetic conditioning.

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          Most cited references 56

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          Cube law, condition factor and weight-length relationships: history, meta-analysis and recommendations

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            Mucins in the mucosal barrier to infection

            The mucosal tissues of the gastrointestinal, respiratory, reproductive, and urinary tracts, and the surface of the eye present an enormous surface area to the exterior environment. All of these tissues are covered with resident microbial flora, which vary considerably in composition and complexity. Mucosal tissues represent the site of infection or route of access for the majority of viruses, bacteria, yeast, protozoa, and multicellular parasites that cause human disease. Mucin glycoproteins are secreted in large quantities by mucosal epithelia, and cell surface mucins are a prominent feature of the apical glycocalyx of all mucosal epithelia. In this review, we highlight the central role played by mucins in accommodating the resident commensal flora and limiting infectious disease, interplay between underlying innate and adaptive immunity and mucins, and the strategies used by successful mucosal pathogens to subvert or avoid the mucin barrier, with a particular focus on bacteria. Supplementary information The online version of this article (doi:10.1038/mi.2008.5) contains supplementary material, which is available to authorized users.
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              On the presence and role of human gene-body DNA methylation

              DNA methylation of promoter sequences is a repressive epigenetic mark that down-regulates gene expression. However, DNA methylation is more prevalent within gene-bodies than seen for promoters, and gene-body methylation has been observed to be positively correlated with gene expression levels. This paradox remains unexplained, and accordingly the role of DNA methylation in gene-bodies is poorly understood. We addressed the presence and role of human gene-body DNA methylation using a meta-analysis of human genome-wide methylation, expression and chromatin data sets. Methylation is associated with transcribed regions as genic sequences have higher levels of methylation than intergenic or promoter sequences. We also find that the relationship between gene-body DNA methylation and expression levels is non-monotonic and bell-shaped. Mid-level expressed genes have the highest levels of gene-body methylation, whereas the most lowly and highly expressed sets of genes both have low levels of methylation. While gene-body methylation can be seen to efficiently repress the initiation of intragenic transcription, the vast majority of methylated sites within genes are not associated with intragenic promoters. In fact, highly expressed genes initiate the most intragenic transcription, which is inconsistent with the previously held notion that gene-body methylation serves to repress spurious intragenic transcription to allow for efficient transcriptional elongation. These observations lead us to propose a model to explain the presence of human gene-body methylation. This model holds that the repression of intragenic transcription by gene-body methylation is largely epiphenomenal, and suggests that gene-body methylation levels are predominantly shaped via the accessibility of the DNA to methylating enzyme complexes.

                Author and article information

                Taylor & Francis
                13 December 2018
                13 December 2018
                : 13
                : 12
                : 1191-1207
                [a ]Centre for Sustainable Aquatic Research, College of Science, Swansea University , Swansea, UK
                [b ]School of Biological Sciences, University of Aberdeen , Aberdeen, UK
                [c ]School of Environmental Sciences, University of East Anglia , Norwich, UK
                [d ]School of Biosciences, Cardiff University , Cardiff, UK
                [e ]Landcatch Natural Selection Ltd, Stirling University Innovation Park , Stirling, UK
                Author notes
                CONTACT Tamsyn M. Uren Webster T.M.UrenWebster@ Centre for Sustainable Aquatic Research, College of Science, Swansea University , Swansea SA2 8PP, UK
                © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License (, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 3, References: 84, Pages: 17
                Funded by: BBSRC-NERC
                Award ID: BB/M026469/1
                This work was funded by a BBSRC-NERC Aquaculture grant (BB/M026469/1) to CGL and by the Welsh Government and Higher Education Funding Council for Wales (HEFCW) through the Sêr Cymru National Research Network for Low Carbon Energy and Environment (NRN-LCEE) to SC.
                Research Paper


                pathogen, immune response, early life, stress, aquaculture, rna-seq, transcriptomics, rrbs, dna methylation


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